The cholinergic anti-inflammatory pathway: A critical review

Autonomic Neuroscience: Basic and Clinical

Volumn 182, Issue , 2014, Pages 65-69

  Martelli, D ^a,b   McKinley, M J ^a   McAllen, R M ^a  

^a UNIVERSITY OF MELBOURNE   (Australia)

^b UNIVERSITY OF BOLOGNA   (Italy)

Author keywords

Vagus inflammation reflex

Indexed keywords

ACETYLCHOLINE; ATROPINE METHYL NITRATE; NICOTINIC RECEPTOR; SEMAPIMOD;

ACTION POTENTIAL; ANTIINFLAMMATORY ACTIVITY; ARTICLE; CHOLINERGIC ANTI INFLAMMATORY PATHWAY; CHOLINERGIC SYSTEM; EFFERENT NERVE; ELECTROSTIMULATION; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PARASYMPATHETIC INNERVATION; PRIORITY JOURNAL; SENSORY NERVE; SYMPATHETIC INNERVATION; SYMPATHETIC NERVE CELL; VAGUS NERVE; VAGUS NERVE STIMULATION; ANIMAL; CHOLINERGIC NERVE CELL; HUMAN; IMMUNOMODULATION; INFLAMMATION; INNERVATION; NERVE TRACT; PATHOPHYSIOLOGY; PHYSIOLOGY; SPLEEN;

ANIMALS; CHOLINERGIC NEURONS; HUMANS; INFLAMMATION; NEURAL PATHWAYS; NEUROIMMUNOMODULATION; SPLEEN; VAGUS NERVE;

EID: 84898858078     PISSN: 15660702     EISSN: 18727484     Source Type: Journal    
DOI: 10.1016/j.autneu.2013.12.007     Document Type: Article

References (37)

1. Andersson U., Tracey K.J. Neural reflexes in inflammation and immunity. J. Exp. Med. 2012, 209:1057-1068.
2. Andersson U., Tracey K.J. Reflex principles of immunological homeostasis. Annu. Rev. Immunol. 2012, 30:313-335.
3. Antonica A., Magni F., Mearini L., Paolocci N. Vagal control of lymphocyte release from rat thymus. J. Auton. Nerv. Syst. 1994, 48:187-197.
4. Bellinger D.L., Lorton D., Hamill R.W., Felten S.Y., Felten D.L. Acetylcholinesterase staining and choline acetyltransferase activity in the young adult rat spleen: lack of evidence for cholinergic innervation. Brain. Behav. Immun. 1993, 7:191-204.
5. Bernik T.R., Friedman S.G., Ochani M., DiRaimo R., Ulloa L., Yang H., Sudan S., Czura C.J., Ivanova S.M., Tracey K.J. Pharmacological stimulation of the cholinergic antiinflammatory pathway. J. Exp. Med. 2002, 195:781-788.
6. Berthoud H.R., Powley T.L. Characterization of vagal innervation to the rat celiac, suprarenal and mesenteric ganglia. J. Auton. Nerv. Syst. 1993, 42:153-169.
7. Berthoud H.R., Carlson N.R., Powley T.L. Topography of efferent vagal innervation of the rat gastrointestinal tract. Am. J. Physiol. 1991, 260:R200-R207.
8. Borovikova L.V., Ivanova S., Nardi D., Zhang M., Yang H., Ombrellino M., Tracey K.J. Role of vagus nerve signaling in CNI-1493-mediated suppression of acute inflammation. Auton. Neurosci. 2000, 85:141-147.
9. Borovikova L.V., Ivanova S., Zhang M., Yang H., Botchkina G.I., Watkins L.R., Wang H., Abumrad N., Eaton J.W., Tracey K.J. Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 2000, 405:458-462.
10. Bratton B.O., Martelli D., McKinley M.J., Trevaks D., Anderson C.R., McAllen R.M. Neural regulation of inflammation: no neural connection from the vagus to splenic sympathetic neurons. Exp. Physiol. 2012, 97:1180-1185.
11. Buijs R.M., van der Vliet J., Garidou M.L., Huitinga I., Escobar C. Spleen vagal denervation inhibits the production of antibodies to circulating antigens. PLoS One 2008, 3:e3152.
12. Caldwell F.T., Graves D.B., Wallace B.H. Humoral versus neural pathways for fever production in rats after administration of lipopolysaccharide. J. Trauma 1999, 47:120-129.
13. Fuentes J.M., Hanly E.J., Aurora A.R., De Maio A., Talamini M.A. Anesthesia-specific protection from endotoxic shock is not mediated through the vagus nerve. Surgery 2005, 138:766-771.
14. Gautron L., Rutkowski J.M., Burton M.D., Wei W., Wan Y., Elmquist J.K. Neuronal and nonneuronal cholinergic structures in the mouse gastrointestinal tract and spleen. J. Comp. Neurol. 2013, 521:3741-3767.
15. Hansen M.K., O'Connor K.A., Goehler L.E., Watkins L.R., Maier S.F. The contribution of the vagus nerve in interleukin-1beta-induced fever is dependent on dose. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2001, 280:R929-R934.
16. Huston J.M., Ochani M., Rosas-Ballina M., Liao H., Ochani K., Pavlov V.A., Gallowitsch-Puerta M., Ashok M., Czura C.J., Foxwell B., Tracey K.J., Ulloa L. Splenectomy inactivates the cholinergic antiinflammatory pathway during lethal endotoxemia and polymicrobial sepsis. J. Exp. Med. 2006, 203:1623-1628.
17. Huston J.M., Wang H., Ochani M., Ochani K., Rosas-Ballina M., Gallowitsch-Puerta M., Ashok M., Yang L., Tracey K.J., Yang H. Splenectomy protects against sepsis lethality and reduces serum HMGB1 levels. J. Immunol. 2008, 181:3535-3539.
18. Izeboud C.A., Mocking J.A., Monshouwer M., van Miert A.S., Witkamp R.F. Participation of beta-adrenergic receptors on macrophages in modulation of LPS-induced cytokine release. J. Recept. Signal Transduct. Res. 1999, 19:191-202.
19. Miao F.J., Janig W., Levine J. Role of sympathetic postganglionic neurons in synovial plasma extravasation induced by bradykinin. J. Neurophys. 1996, 75:715-724.
20. Nance D.M., Sanders V.M. Autonomic innervation and regulation of the immune system (1987-2007). Brain Behav. Immun. 2007, 21:736-745.
21. Nathan C. Points of control in inflammation. Nature 2002, 420:846-852.
22. Olofsson P.S., Rosas-Ballina M., Levine Y.A., Tracey K.J. Rethinking inflammation: neural circuits in the regulation of immunity. Immunol. Rev. 2012, 248:188-204.
23. Ootsuka Y., Blessing W.W., Steiner A.A., Romanovsky A.A. Fever response to intravenous prostaglandin E2 is mediated by the brain but does not require afferent vagal signaling. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2008, 294:R1294-R1303.
24. Pabst R. The spleen in lymphocyte migration. Immunol. Today 1988, 9:43-45.
25. Pavlov V.A., Wang H., Czura C.J., Friedman S.G., Tracey K.J. The cholinergic anti-inflammatory pathway: a missing link in neuroimmunomodulation. Mol. Med. 2003, 9:125-134.
26. Pavlov V.A., Ochani M., Gallowitsch-Puerta M., Ochani K., Huston J.M., Czura C.J., Al-Abed Y., Tracey K.J. Central muscarinic cholinergic regulation of the systemic inflammatory response during endotoxemia. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:5219-5223.
27. Rhen T., Cidlowski J.A. Antiinflammatory action of glucocorticoids-new mechanisms for old drugs. N. Engl. J. Med. 2005, 353:1711-1723.
28. Rogausch H., Zwingmann D., Trudewind M., del Rey A., Voigt K.H., Besedovsky H. Local and systemic autonomic nervous effects on cell migration to the spleen. J. Appl. Physiol. 2003, 94:469-475.
29. Romanovsky A.A., Almeida M.C., Aronoff D.M., Ivanov A.I., Konsman J.P., Steiner A.A., Turek V.F. Fever and hypothermia in systemic inflammation: recent discoveries and revisions. Front. Biosci. 2005, 10:2193-2216.
30. Rosas-Ballina M., Tracey K.J. Cholinergic control of inflammation. J. Intern. Med. 2009, 265:663-679.
31. Rosas-Ballina M., Ochani M., Parrish W.R., Ochani K., Harris Y.T., Huston J.M., Chavan S., Tracey K.J. Splenic nerve is required for cholinergic antiinflammatory pathway control of TNF in endotoxemia. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:11008-11013.
32. Rosas-Ballina M., Olofsson P.S., Ochani M., Valdes-Ferrer S.I., Levine Y.A., Reardon C., Tusche M.W., Pavlov V.A., Andersson U., Chavan S., Mak T.W., Tracey K.J. Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit. Science 2011, 334:98-101.
33. Saper C.B., Romanovsky A.A., Scammell T.E. Neural circuitry engaged by prostaglandins during the sickness syndrome. Nat. Neurosci. 2012, 15:1088-1095.
34. Sternberg E.M. Neural regulation of innate immunity: a coordinated nonspecific host response to pathogens. Nat. Rev. Immunol. 2006, 6:318-328.
35. Tracey K.J. The inflammatory reflex. Nature 2002, 420:853-859.
36. Vida G., Pena G., Deitch E.A., Ulloa L. alpha7-cholinergic receptor mediates vagal induction of splenic norepinephrine. J. Immunol. 2011, 186:4340-4346.
37. Wang H., Yu M., Ochani M., Amella C.A., Tanovic M., Susarla S., Li J.H., Wang H., Yang H., Ulloa L., Al-Abed Y., Czura C.J., Tracey K.J. Nicotinic acetylcholine receptor alpha7 subunit is an essential regulator of inflammation. Nature 2003, 421:384-388.